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Repeat-based holocentromeres influence genome architecture and karyotype evolution

2022; Cell Press; Volume: 185; Issue: 17 Linguagem: Inglês

10.1016/j.cell.2022.06.045

1097-4172

Paulo G. Hofstatter, Gokilavani Thangavel, Thomas Lux, Pavel Neumann, Tihana Vondrak, Petr Novák, Meng Zhang, Lucas Costa, Marco Castellani, Alison Scott, Helena Toegelová, Jörg Fuchs, Yennifer Mata‐Sucre, Yhanndra Dias, André Luís Laforga Vanzela, Bruno Hüettel, Cícero Almeida, Hana Šimková, Gustavo Souza, Andrea Pedrosa‐Harand, Jir̆ı́ Macas, Klaus Mayer, Andreas Houben, André Marques,

Genetic diversity and population structure

The centromere represents a single region in most eukaryotic chromosomes. However, several plant and animal lineages assemble holocentromeres along the entire chromosome length. Here, we compare genome organization and evolution as a function of centromere type by assembling chromosome-scale holocentric genomes with repeat-based holocentromeres from three beak-sedge (Rhynchospora pubera, R. breviuscula, and R. tenuis) and their closest monocentric relative, Juncus effusus. We demonstrate that transition to holocentricity affected 3D genome architecture by redefining genomic compartments, while distributing centromere function to thousands of repeat-based centromere units genome-wide. We uncover a complex genome organization in R. pubera that hides its unexpected octoploidy and describe a marked reduction in chromosome number for R. tenuis, which has only two chromosomes. We show that chromosome fusions, facilitated by repeat-based holocentromeres, promoted karyotype evolution and diploidization. Our study thus sheds light on several important aspects of genome architecture and evolution influenced by centromere organization.